Abstract
Regulatory elements of the maize rbcS-m3 gene (a member of the family of genes encoding the small subunit of ribulose bisphosphate carboxylase) that are sufficient for expression of the β-glucuronidase (gusA) gene in photosynthetic tissue lead to relatively weak expression of the reporter gene in epidermal cells of green maize leaves when delivered by ballistic gene transfer methods. However, epidermal cells of white, immature segments of maize leaf bases express the same reporter gene strongly. Morphologically, these epidermal cells look undifferentiated and are uniform in size and shape. When cultured for seven days on Murashige-Skoog medium [18], exised leaf base segments expand two- to threefold, and epidermal and guard cells differentiate and mature, regardless of whether or not the tissue is illuminated. Epidermal cells that differentiate in darkness continue to have the capacity to express the rbcS-m3:: gusA reporter gene strongly. However, if the leaf base segments are illuminated after four to five days of expansion in darkness, but not before, these more mature epidermal cells are largely unable to express the same gene. That is, they acquire the characteristics of epidermal cells of green maize leaves with regard to expressing the rbcS-m3 reporter gene after undergoing a developmental program (in light or darkness) in vitro and after being exposed to light. White light but not red is effective. Suppression of expression in maize epidermal cells requires different rbcS-m3 sequences than in mesophyll cells [31].
Similar content being viewed by others
References
Bansal KC, Viret J-F, Haley J, Khan JM, Schantz R, Bogorad L: Transient expression from cab-m1 and rbcS-m3 promoter sequences is different in mesophyll and bundle sheath cells in maize leaves. Proc Natl Acad Sci USA 89: 3654–3658 (1992).
Berry JO, Breding DE, Klessig DF: Light-mediated control of translational initiation of ribulose-1,5-bisphosphate carboxylase in amaranth cotyledons. Plant Cell 2: 795–803 (1990).
Broglie R, Coruzzi G, Keith B, Chua N-H: Molecular biology of C4 photosynthesis in Zea Mays: differential localization of proteins and mRNAs in the two leaf cell types. Plant Mol Biol 3: 431–444 (1984).
Chandler VL, Radicella JP, Robbins TP, Chen J, Turks D: Two regulatory genes of the maize anthocyanin pathway are homologous: Isolation of B using R genomic sequences. Plant Cell 1: 1175–1183 (1989).
Edwards JW, Coruzzi GM: Cell-specific gene expression in plants. Annu Rev Genet 24: 275–303 (1990).
Esau K: Anatomy of Seed Plants. John Wiley, New York (1977).
Finer JJ, Vain P, Jones MW, McMullen MD: Development of the particle inflow gun for DNA delivery to plant cells. Plant Cell Rep 11: 323–328 (1992).
Freeling M: A conceptual framework for maize leaf development. Devel Biol 153: 44–58 (1992).
Gilmartin PM, Sarokin L, Memelink J, Chua N-H: Molecular light switches for plant genes. Plant Cell 2: 369–378 (1990).
Goff SA, Klein TM, Roth BA, Fromm ME, Cone KC, Radicella JP, Chandler VL: Transactivation of anthocyanin biosynthetic genes following transfer of B regulatory genes into maize tissues. EMBO J 9: 2517–2522 (1990).
Huber SC, Hall TC, Edwards GE: Differential localization of fraction I protein between chloroplast types. Plant Physiol 57: 730–733 (1976).
Jefferson RA: Assaying chimeric genes in plants: the GUS gene fusion system. Plant Mol Biol Rep 5: 387–405 (1987).
Langdale JA, Zelitch I, Miller E, Nelson T: Cell position and light influence C4 vs. C3 patterns of photosynthetic gene expression in maize. EMBO J 7: 3643–3651 (1988).
Langdale JA, Rothermel A, Nelson T: Cellular pattern of photosynthetic gene expression in developing maize leaves. Genes Devel 2: 106–115 (1988).
Lebrun M, Waksman G, Freyssinet G: Nucleotide sequence of a gene encoding corn ribulose-1,5-bisphosphate carboxylase/oxygenase small subunit (rbcS). Nucl Acids Res 15: 4360 (1987).
Link G, Coen DM, Bogorad L: Differential expression of the gene for the large subunit of ribulose bisphosphate bisphosphate carboxylase in maize leaf cell types. Cell 15: 725–731 (1978).
Mendel RR, Müller B, Schulze J, Kolesnikov V, Zelenin A: Delivery of foreign genes to intact barley cells by high-velocity microprojectiles. Theor Appl Genet 78: 31–34 (1989).
Murashige T, Skoog F: A revised medium for rapid growth and bioassay with tobacco tissue cultures. Physiol Plant 15: 473–497 (1962).
Nelson T, Harpster MH, Mayfield SP, Taylor WC: Lightregulated gene expression during maize leaf development. J Cell Biol 98: 558–564 (1984).
Poethig RS: Phase change and the regulation of shoot morphogenesis in plants. Science 250: 923–930 (1990).
Purcell M, Mabrouk YM, Bogorad L: Red far-red and blue light-responsive regions of maize rbcS-m3 are active in bundle sheath and mesophyll cells, respectively. Proc Natl Acad Sci USA 92: 11504–11508 (1995).
Schäffner AR, Sheen J-Y: Maize rbcS promoter activity depends on sequence elements not found in dicot rbcS promoters. Plant Cell 3: 997–1012 (1991).
Sharman BC: Developmental anatomy of the shoot of Zea mays L. Ann Bot 6: 245–284 (1942).
Sheen J-Y, Bogorad L: Differential expression of the ribulose bisphosphate carboxylase large subunit gene in bundle sheath and mesophyll cells in developing maize leaves is influenced by light. Plant Physiol 79: 1072–1076 (1985).
Sheen J-Y, Bogorad L: Expression of the ribulose-1,5-bisphosphate carboxylase large subunit gene and three small subunit genes in two cell types of maize leaves. EMBO J 5: 3417–3422 (1986).
Stebbins GL, Shah SS: Developmental studies of cell differentiation in the epidermis of monocotyledons. Devel Biol 2: 477–500 (1960).
Taylor WC: Regulatory interactions between nuclear and plastid genomes. Annu Rev Plant Physiol Plant Mol Biol 40: 211–233 (1989).
Thompson WF, White MJ: Physiological and molecular studies of light-regulated nuclear genes in higher plants. Annu Rev Plant Physiol Plant Mol Biol 42: 423–466 (1991).
Thompson DM, Tanzer MM, Meagher RB: Degradation products of the mRNA encoding the small subunit of ribulose-1,5-bisphosphate carboxylase in soybean and transgenic petunia. Plant Cell 4: 47–58 (1992).
Vain P, McMullen MD, Finer JJ: Osmotic treatment enhances particle bombardment-mediated transient and stable transformation of maize. Plant Cell Rep 12: 84–88 (1993).
Viret J-F, Mabrouk Y, Bogorad L: Transcriptional photoregulation of cell-type preferred expression of maize rbcS-m3: 3′ and 5′ sequences are involved. Proc Natl Acad Sci USA 91: 8577–8581 (1994).
Wanner LA, Gruissem W: Expression dynamics of the tomato rbcS gene family during development. Plant Cell 3: 1289–1303 (1991).
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Bilang, R., Bogorad, L. Light-dependent developmental control of rbcS gene expression in epidermal cells of maize leaves. Plant Mol Biol 31, 831–841 (1996). https://doi.org/10.1007/BF00019470
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00019470